Gliomas Interact with Non-glioma Brain Cells via Extracellular Vesicles

被引:67
作者
Gao, Xiaofei [1 ,2 ]
Zhang, Zhaohuan [1 ,2 ,3 ]
Mashimo, Tomoyuki [4 ]
Shen, Bo [1 ,2 ]
Nyagilo, James [5 ]
Wang, Hao [1 ,2 ]
Wang, Yihui [1 ,2 ,6 ]
Liu, Zhida [7 ]
Mulgaonkar, Aditi [8 ]
Hu, Xiao-Ling [1 ,2 ]
Piccirillo, Sara G. M. [4 ]
Eskiocak, Ugur [1 ,2 ]
Dave, Digant P. [9 ]
Qin, Song [10 ]
Yang, Yongjie [11 ]
Sun, Xiankai [8 ]
Fu, Yang-Xin [7 ]
Zong, Hui [12 ]
Sun, Wenzhi [13 ,14 ]
Bachoo, Robert M. [4 ,5 ,15 ,16 ]
Ge, Woo-Ping [1 ,2 ,5 ,16 ]
机构
[1] Univ Texas Southwestern Med Ctr Dallas, Childrens Res Inst, Dallas, TX 75390 USA
[2] Univ Texas Southwestern Med Ctr Dallas, Dept Pediat, Dallas, TX 75390 USA
[3] Second Mil Med Univ, Changzheng Hosp, Dept Neurol, Shanghai 200003, Peoples R China
[4] Univ Texas Southwestern Med Ctr Dallas, Dept Internal Med, Dallas, TX 75390 USA
[5] Univ Texas Southwestern Med Ctr Dallas, Dept Neurol & Neurotherapeut, Dallas, TX 75390 USA
[6] Huazhong Univ Sci & Technol, Tongji Hosp, Tongji Med Coll, Wuhan 4300030, Hubei, Peoples R China
[7] Univ Texas Southwestern Med Ctr Dallas, Dept Pathol, Dallas, TX 75390 USA
[8] Univ Texas Southwestern Med Ctr Dallas, Dept Radiol, Dallas, TX 75390 USA
[9] Univ Texas Arlington, Dept Bioengn, Arlington, TX 76010 USA
[10] Fudan Univ, Sch Basic Med Sci, Dept Anat Histol & Embryol, Shanghai 200032, Peoples R China
[11] Tufts Univ, Sch Med, Grad Sch Biomed Sci, Dept Neurosci, Boston, MA 02111 USA
[12] Univ Virginia, Dept Microbiol Immunol & Canc Biol, Charlottesville, VA 22908 USA
[13] Chinese Inst Brain Res, Beijing 102206, Peoples R China
[14] Capital Med Univ, Sch Basic Med Sci, Beijing 100069, Peoples R China
[15] Univ Texas Southwestern Med Ctr Dallas, Harold C Simmons Comprehens Canc Ctr, Dallas, TX 75390 USA
[16] Univ Texas Southwestern Med Ctr Dallas, Dept Neurosci, Dallas, TX 75390 USA
基金
中国国家自然科学基金;
关键词
STEM-CELL; ORIGIN; ASTROCYTES; GROWTH; MICROGLIA; MECHANISM; PROTEINS; PROLIFERATION; COMMUNICATION; INVASIVENESS;
D O I
10.1016/j.celrep.2020.01.089
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Emerging evidence suggests that crosstalk between glioma cells and the brain microenvironment may influence brain tumor growth. To date, known reciprocal interactions among these cells have been limited to the release of paracrine factors. Combining a genetic strategy with longitudinal live imaging, we find that individual gliomas communicate with distinct sets of non-glioma cells, including glial cells, neurons, and vascular cells. Transfer of genetic material is achieved mainly through extracellular vesicles (EVs), although cell fusion also plays a minor role. We further demonstrate that EV-mediated communication leads to the increase of synaptic activity in neurons. Blocking EV release causes a reduction of glioma growth in vivo. Our findings indicate that EV-mediated interaction between glioma cells and non-glioma brain cells alters the tumor microenvironment and contributes to glioma development.
引用
收藏
页码:2489 / +
页数:17
相关论文
共 71 条
[41]   BRAF Mutation and CDKN2A Deletion Define a Clinically Distinct Subgroup of Childhood Secondary High-Grade Glioma [J].
Mistry, Matthew ;
Zhukova, Nataliya ;
Merico, Daniele ;
Rakopoulos, Patricia ;
Krishnatry, Rahul ;
Shago, Mary ;
Stavropoulos, James ;
Alon, Noa ;
Pole, Jason D. ;
Ray, Peter N. ;
Navickiene, Vilma ;
Mangerel, Joshua ;
Remke, Marc ;
Buczkowicz, Pawel ;
Ramaswamy, Vijay ;
Stucklin, Ana Guerreiro ;
Li, Martin ;
Young, Edwin J. ;
Zhang, Cindy ;
Castelo-Branco, Pedro ;
Bakry, Doua ;
Laughlin, Suzanne ;
Shlien, Adam ;
Chan, Jennifer ;
Ligon, Keith L. ;
Rutka, James T. ;
Dirks, Peter B. ;
Taylor, Michael D. ;
Greenberg, Mark ;
Malkin, David ;
Huang, Annie ;
Bouffet, Eric ;
Hawkins, Cynthia E. ;
Tabori, Uri .
JOURNAL OF CLINICAL ONCOLOGY, 2015, 33 (09) :1015-+
[42]   Astrocytes and disease: a neurodevelopmental perspective [J].
Molofsky, Anna V. ;
Krenick, Robert ;
Ullian, Erik ;
Tsai, Hui-hsin ;
Deneen, Benjamin ;
Richardson, William D. ;
Barres, Ben A. ;
Rowitch, David H. .
GENES & DEVELOPMENT, 2012, 26 (09) :891-907
[43]   Extracellular vesicles in the biology of brain tumour stem cells - Implications for inter-cellular communication, therapy and biomarker development [J].
Nakanoa, Ichiro ;
Garnier, Delphine ;
Minata, Mutsuko ;
Rak, Janusz .
SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY, 2015, 40 :17-26
[44]   Brain tumour cells interconnect to a functional and resistant network [J].
Osswald, Matthias ;
Jung, Erik ;
Sahm, Felix ;
Solecki, Gergely ;
Venkataramani, Varun ;
Blaes, Jonas ;
Weil, Sophie ;
Horstmann, Heinz ;
Wiestler, Benedikt ;
Syed, Mustafa ;
Huang, Lulu ;
Ratliff, Miriam ;
Jazi, Kianush Karimian ;
Kurz, Felix T. ;
Schmenger, Torsten ;
Lemke, Dieter ;
Goemmel, Miriam ;
Pauli, Martin ;
Liao, Yunxiang ;
Haering, Peter ;
Pusch, Stefan ;
Herl, Verena ;
Steinhaeuser, Christian ;
Krunic, Damir ;
Jarahian, Mostafa ;
Miletic, Hrvoje ;
Berghoff, Anna S. ;
Griesbeck, Oliver ;
Kalamakis, Georgios ;
Garaschuk, Olga ;
Preusser, Matthias ;
Weiss, Samuel ;
Liu, Haikun ;
Heiland, Sabine ;
Platten, Michael ;
Huber, Peter E. ;
Kuner, Thomas ;
von Deimling, Andreas ;
Wick, Wolfgang ;
Winkler, Frank .
NATURE, 2015, 528 (7580) :93-+
[45]   Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma [J].
Patel, Anoop P. ;
Tirosh, Itay ;
Trombetta, John J. ;
Shalek, Alex K. ;
Gillespie, Shawn M. ;
Wakimoto, Hiroaki ;
Cahill, Daniel P. ;
Nahed, Brian V. ;
Curry, William T. ;
Martuza, Robert L. ;
Louis, David N. ;
Rozenblatt-Rosen, Orit ;
Suva, Mario L. ;
Regev, Aviv ;
Bernstein, Bradley E. .
SCIENCE, 2014, 344 (6190) :1396-1401
[46]   Non-Stem Cell Origin for Oligodendroglioma [J].
Persson, Anders I. ;
Petritsch, Claudia ;
Swartling, Fredrik J. ;
Itsara, Melissa ;
Sim, Fraser J. ;
Auvergne, Romane ;
Goldenberg, David D. ;
Vandenberg, Scott R. ;
Nguyen, Kim N. ;
Yakovenko, Stanislava ;
Ayers-Ringler, Jennifer ;
Nishiyama, Akiko ;
Stallcup, William B. ;
Berger, Mitchel S. ;
Bergers, Gabriele ;
McKnight, Tracy R. ;
Goldman, Steven A. ;
Weiss, William A. .
CANCER CELL, 2010, 18 (06) :669-682
[47]   The role of astrocytes in the progression of brain cancer: complicating the picture of the tumor microenvironment [J].
Placone, Amanda L. ;
Quiones-Hinojosa, Alfredo ;
Searson, Peter C. .
TUMOR BIOLOGY, 2016, 37 (01) :61-69
[48]   Emerging Roles of Extracellular Vesicles in the Nervous System [J].
Rajendran, Lawrence ;
Bali, Jitin ;
Barr, Maureen M. ;
Court, Felipe A. ;
Kramer-Albers, Eva-Maria ;
Picou, Frederic ;
Raposo, Graca ;
van der Vos, Kristan E. ;
van Nie, Guillaume ;
Wang, Juan ;
Breakefield, Xandra O. .
JOURNAL OF NEUROSCIENCE, 2014, 34 (46) :15482-15489
[49]   Astrocytes Enhance the Invasion Potential of Glioblastoma Stem-Like Cells [J].
Rath, Barbara H. ;
Fair, Joshlean M. ;
Jamal, Muhammad ;
Camphausen, Kevin ;
Tofilon, Philip J. .
PLOS ONE, 2013, 8 (01)
[50]   Extracellular Vesicle-Mediated Transfer of Genetic Information between the Hematopoietic System and the Brain in Response to Inflammation [J].
Ridder, Kirsten ;
Keller, Sascha ;
Dams, Maria ;
Rupp, Anne-Kathleen ;
Schlaudraff, Jessica ;
Del Turco, Domenico ;
Starmann, Julia ;
Macas, Jadranka ;
Karpova, Darja ;
Devraj, Kavi ;
Depboylu, Candan ;
Landfried, Britta ;
Arnold, Bernd ;
Plate, Karl H. ;
Hoeglinger, Guenter ;
Sueltmann, Holger ;
Altevogt, Peter ;
Momma, Stefan .
PLOS BIOLOGY, 2014, 12 (06)